A descending pathway facilitates undulatory wave propagation inCaenorhabditis elegansthrough gap junctions

• DOI: 10.1101/131490
• Publication Date: 2017-06-18T05:10:11Z
• Authors: Tianqi Xu; Jing Huo; Shuai Shao; Michelle Po; Taizo Kawano; Yangning Lu; Min Wu; Mei Zhen; Quan Wen
• Keywords: Motor Neurons; 0303 health sciences; Behavior, Animal; Gap Junctions; Motor Activity; Animals, Genetically Modified; Optogenetics; 03 medical and health sciences; Interneurons; Animals; Calcium; Caenorhabditis elegans; Caenorhabditis elegans Proteins; Locomotion

Descending signals from the brain play critical roles in controlling and modulating locomotion kinematics. In theCaenorhabditis elegansnervous system, descending AVB premotor interneurons exclusively form gap junctions with B-type motor neurons that drive forward locomotion. We combined genetic analysis, optogenetic manipulation, and computational modeling to elucidate the function of AVB-B gap junctions during forward locomotion. First, we found that some B-type motor neurons generated intrinsic rhythmic activity, constituting distributed central pattern generators. Second, AVB premotor interneurons drove bifurcation of B-type motor neuron dynamics, triggering their transition from stationary to oscillatory activity. Third, proprioceptive couplings between neighboring B-type motor neurons entrained the frequency of body oscillators, forcing coherent propagation of bending waves. Despite substantial anatomical differences between the worm motor circuit and those in higher model organisms, we uncovered converging principles that govern coordinated locomotion.Significance StatementA deep understanding of the neural basis of motor behavior must integrate neuromuscular dynamics, mechanosensory feedback, as well as global command signals, to predict behavioral dynamics. Here, we report on an integrative approach to defining the circuit logic underlying coordinated locomotion inC. elegans.Our combined experimental and computational analysis revealed that (1) motor neurons inC. eleganscould function as intrinsic oscillators; (2) Descending inputs and proprioceptive couplings work synergistically to facilitate the sequential activation of motor neuron activities, allowing bending waves to propagate efficiently along the body. Our work thus represents a key step towards an integrative view of animal locomotion.